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Coupling Between and Among Ammonia Oxidizers and Nitrite Oxidizers in Grassland Mesocosms Submitted to Elevated CO2 and Nitrogen Supply

  • Soil Microbiology
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Abstract

Many studies have assessed the responses of soil microbial functional groups to increases in atmospheric CO2 or N deposition alone and more rarely in combination. However, the effects of elevated CO2 and N on the (de)coupling between different microbial functional groups (e.g., different groups of nitrifiers) have been barely studied, despite potential consequences for ecosystem functioning. Here, we investigated the short-term combined effects of elevated CO2 and N supply on the abundances of the four main microbial groups involved in soil nitrification: ammonia-oxidizing archaea (AOA), ammonia-oxidizing bacteria (AOB), and nitrite-oxidizing bacteria (belonging to the genera Nitrobacter and Nitrospira) in grassland mesocosms. AOB and AOA abundances responded differently to the treatments: N addition increased AOB abundance, but did not alter AOA abundance. Nitrobacter and Nitrospira abundances also showed contrasted responses to the treatments: N addition increased Nitrobacter abundance, but decreased Nitrospira abundance. Our results support the idea of a niche differentiation between AOB and AOA, and between Nitrobacter and Nitrospira. AOB and Nitrobacter were both promoted at high N and C conditions (and low soil water content for Nitrobacter), while AOA and Nitrospira were favored at low N and C conditions (and high soil water content for Nitrospira). In addition, Nitrobacter abundance was positively correlated to AOB abundance and Nitrospira abundance to AOA abundance. Our results suggest that the couplings between ammonia and nitrite oxidizers are influenced by soil N availability. Multiple environmental changes may thus elicit rapid and contrasted responses between and among the soil ammonia and nitrite oxidizers due to their different ecological requirements.

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References

  1. Barnard RL, Leadley PW, Hungate BA (2005) Global change, nitrification and denitrification: a review. Glob Biogeochem Cycles. doi:10.1029/2004GB002282

    Google Scholar 

  2. Cantarel AAM, Bloor JMG, Pommier T, Guillaumaud N, Moirot C, Soussana JF, Poly F (2012) Four years of experimental climate change modifies the microbial drivers of N2O fluxes in an upland grassland ecosystem. Glob Chang Biol 18:2520–2531

    Article  Google Scholar 

  3. Gutknecht JLM, Field CB, Balser TC (2012) Microbial communities and their responses to simulated global change fluctuate greatly over multiple years. Glob Chang Biol 18:2256–2269

    Article  Google Scholar 

  4. Henry HAL, Juarez JD, Field CB, Vitousek PM (2005) Interactive effects of elevated CO2 N deposition and climate change on extracellular enzyme activity and soil density fractionation in a California annual grassland. Glob Chang Biol 11:1808–1815

    Article  Google Scholar 

  5. Kandeler E, Mosier AR, Morgan JA, Milchunas DG, King JY, Rudolph S, Tscherko D (2008) Transient elevation of carbon dioxide modifies the microbial community composition in a semi-arid grassland. Soil Biol Biochem 40:162–171

    Article  CAS  Google Scholar 

  6. Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai Z, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA (2008) Transformation of the nitrogen cycle: recent trends questions and potential solutions. Science 320:889–892

    Article  CAS  PubMed  Google Scholar 

  7. IPCC et al (2007) Climate change 2007: the physical science basis. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M (eds) Contribution of working group I to the fourth assessment report of the IPCC. Cambridge University Press, Cambridge, p 1009

    Google Scholar 

  8. Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol. doi:10.3389/fmicb.2012.00348

    PubMed Central  PubMed  Google Scholar 

  9. Griffiths BS, Philippot L (2012) Insights into the resistance and resilience of the soil microbial community. FEMS Microbiol Rev 37:112–129

    Article  PubMed  Google Scholar 

  10. Wertz S, Degrange V, Prosser JI, Poly F, Commeaux C, Guillaumaud N, Le Roux X (2007) Decline of soil microbial diversity does not influence the resistance and resilience of key soil microbial functional groups following a model disturbance. Environ Microbiol 9:2211–2219

    Article  PubMed  Google Scholar 

  11. Boudsocq S, Niboyet A, Lata JC, Raynaud X, Loeuille N, Mathieu J, Blouin M, Abbadie L, Barot S (2012) Plant preference for ammonium versus nitrate: a neglected determinant of ecosystem functioning? Am Nat 180:60–69

    Article  CAS  PubMed  Google Scholar 

  12. Hodge A, Robinson D, Fitter A (2000) Are microorganisms more effective than plants at competing for nitrogen? Trends Plant Sci 5:304–308

    Article  CAS  PubMed  Google Scholar 

  13. Wrage N, Velthof GL, Van Beusichem ML, Oenema O (2001) Role of nitrifier denitrification in the production of nitrous oxide. Soil Biol Biochem 33:1723–1732

    Article  CAS  Google Scholar 

  14. Hayatsu M, Tago K, Saito M (2008) Various players in the nitrogen cycle: diversity and functions of the microorganisms involved in nitrification and denitrification. Soil Sci Plant Nutr 54:33–45

    Article  CAS  Google Scholar 

  15. Freitag TE, Chang L, Clegg CD, Prosser JI (2005) Influence of inorganic nitrogen management regime on the diversity of nitrite-oxidizing bacteria in agricultural grassland soils. Appl Environ Microbiol 71:8323–8334

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Horz HP, Barbrook A, Field CB, Bohannan BJM (2004) Ammonia-oxidizing bacteria respond to multifactorial global change. Proc Natl Acad Sci USA 101:15136–15141

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Regan K, Kammann C, Hartung K, Lenhart K, Muller C, Philippot L, Kandeler E, Marhan S (2011) Can differences in microbial abundances help explain enhanced N2O emissions in a permanent grassland under elevated atmospheric CO2? Glob Chang Biol 17:3176–3186

    Article  Google Scholar 

  18. Chen YL, Hu HW, Han HY, Du Y, Wan SQ, Xu ZW, Chen BD (2014) Abundance and community structure of ammonia‐oxidizing archaea and bacteria in response to fertilization and mowing in a temperate steppe in Inner Mongolia. FEMS Microbiol Ecol. doi:10.1111/1574-6941.12336

    Google Scholar 

  19. Daebeler A, Abell GC, Bodelier PL, Bodrossy L, Frampton DM, Hefting MM, Laanbroek HJ (2012) Archaeal dominated ammonia-oxidizing communities in Icelandic grassland soils are moderately affected by long-term N fertilization and geothermal heating. Front Microbiol. doi:10.3389/fmicb.2012.00352

    PubMed Central  PubMed  Google Scholar 

  20. Dai Y, Di HJ, Cameron KC, He JZ (2013) Effects of nitrogen application rate and a nitrification inhibitor dicyandiamide on ammonia oxidizers and N2O emissions in a grazed pasture soil. Sci Total Environ 465:125–135

    Article  CAS  PubMed  Google Scholar 

  21. Di HJ, Cameron KC, Shen JP, Winefield CS, O’Callaghan M, Bowatte S, He JZ (2010) Ammonia‐oxidizing bacteria and archaea grow under contrasting soil nitrogen conditions. FEMS Microbiol Ecol 72:386–394

    Article  CAS  PubMed  Google Scholar 

  22. Docherty KM, Balser TC, Bohannan BJM, Gutknecht JLM (2012) Soil microbial responses to fire and interacting global change factors in a California annual grassland. Biogeochemistry 109:63–83

    Article  CAS  Google Scholar 

  23. Hartmann AA, Barnard RL, Marhan S, Niklaus PA (2013) Effects of drought and N-fertilization on N cycling in two grassland soils. Oecologia 171:705–717

    Article  PubMed  Google Scholar 

  24. O’Callaghan M, Gerard EM, Carter PE, Lardner R, Sarathchandra U, Burch G et al (2010) Effect of the nitrification inhibitor dicyandiamide (DCD) on microbial communities in a pasture soil amended with bovine urine. Soil Biol Biochem 42:1425–1436

    Article  Google Scholar 

  25. Shen XY, Zhang LM, Shen JP, Li LH, Yuan CL, He JZ (2011) Nitrogen loading levels affect abundance and composition of soil ammonia oxidizing prokaryotes in semiarid temperate grassland. J Soils Sediments 11:1243–1252

    Article  CAS  Google Scholar 

  26. Tian XF, Hu HW, Ding Q, Song MH, Xu XL, Zheng Y, Guo LD (2013) Influence of nitrogen fertilization on soil ammonia oxidizer and denitrifier abundance microbial biomass and enzyme activities in an alpine meadow. Biol Fertil Soils. doi:10.1007/s00374-013-0889-0

    Google Scholar 

  27. Zhang X, Liu W, Schloter M, Zhang G, Chen Q, Huang J, Li L, Elser JJ, Han X (2013) Response of the abundance of key soil microbial nitrogen-cycling genes to multi-factorial global changes. PLoS One. doi:10.1371/journal.pone.0076500

    Google Scholar 

  28. Kowalchuk GA, Stephen JR (2001) Ammonia-oxidizing bacteria: a model for molecular microbial ecology. Annu Rev Microbiol 55:485–529

    Article  CAS  PubMed  Google Scholar 

  29. Burns LC, Stevens RJ, Laughlin RJ (1996) Production of nitrite in soil by simultaneous nitrification and denitrification. Soil Biol Biochem 28:609–616

    Article  CAS  Google Scholar 

  30. Gelfand I, Yakir D (2008) Influence of nitrite accumulation in association with seasonal patterns and mineralization of soil nitrogen in a semi-arid pine forest. Soil Biol Biochem 40:415–424

    Article  CAS  Google Scholar 

  31. Roux-Michollet D, Czarnes S, Adam B, Berry D, Commeaux C, Guillaumaud N, Le Roux X, Clays-Josserand A (2008) Effects of steam disinfestation on community structure abundance and activity of heterotrophic denitrifying and nitrifying bacteria in an organic farming soil. Soil Biol Biochem 40:1836–1845

    Article  CAS  Google Scholar 

  32. Niboyet A, Le Roux X, Dijkstra P, Hungate BA, Barthes L, Blankinship JC, Brown JR, Field CB, Leadley PW (2011) Testing interactive effects of global environmental changes on soil nitrogen cycling. Ecosphere 2:1–24

    Article  Google Scholar 

  33. Zhang L-M, Offre PR, He J-Z, Verhamme DT, Nicol GW, Prosser JI (2010) Autotrophic ammonia oxidation by soil thaumarchaea. Proc Natl Acad Sci U S A 107:17240–17245

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  34. Degrange V, Lensi R, Bardin R (1997) Activity size and structure of a Nitrobacter community as affected by organic carbon and nitrite in sterile soil. FEMS Microbiol Ecol 24:173–180

    Article  CAS  Google Scholar 

  35. Hatzenpichler R (2012) Diversity physiology and niche differentiation of ammonia-oxidizing archaea. Appl Environ Microbiol 78:7501–7510

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Prosser JI, Nicol GW (2012) Archaeal and bacterial ammonia-oxidisers in soil: the quest for niche specialisation and differentiation. Trends Microbiol 20:523–531

    Article  CAS  PubMed  Google Scholar 

  37. Xie Z, Le Roux X, Wang C, Gu Z, An M, Nan H, Li F, Du G, Feng H, Ma X (2014) Identifying response groups of soil nitrifiers and denitrifiers to grazing and associated soil environmental drivers in Tibetan alpine meadows. Soil Biol Biochem 77:89–99

    Article  CAS  Google Scholar 

  38. Attard E, Poly F, Commeaux C, Laurent F, Terada A, Smets BF, Recous S, Le Roux X (2010) Shifts between Nitrospira- and Nitrobacter-like nitrite oxidizers underlie the response of soil potential nitrite oxidation to changes in tillage practices. Environ Microbiol 12:315–326

    Article  CAS  PubMed  Google Scholar 

  39. Niboyet A, Barthes L, Hungate BA, Le Roux X, Bloor JMG, Ambroise A, Fontaine S, Price PM, Leadley PW (2010) Responses of soil nitrogen cycling to the interactive effects of elevated CO2 and inorganic N supply. Plant Soil 327:35–47

    Article  CAS  Google Scholar 

  40. Bloor JM, Niboyet A, Leadley PW, Barthes L (2009) CO2 and inorganic N supply modify competition for N between co-occurring grass plants, tree seedlings and soil microorganisms. Soil Biol Biochem 41:544–552

    Article  CAS  Google Scholar 

  41. Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660

    Article  Google Scholar 

  42. Holland EA, Braswell B, Lamarque J-F, Townsend A, Sulzman J, Müller J-F, Dentener F, Brasseur G, Levy H II, Penner JE (1997) Variations in the predicted spatial distribution of atmospheric nitrogen deposition and their impact on carbon uptake by terrestrial ecosystems. J Geophys Res 102:15849–15815

    Article  CAS  Google Scholar 

  43. Tourna M, Freitag TE, Nicol GW, Prosser JI (2008) Growth activity and temperature responses of ammonia-oxidizing archaea and bacteria in soil microcosms. Environ Microbiol 10:1357–1364

    Article  CAS  PubMed  Google Scholar 

  44. Rotthauwe JH, Witzel KP, Liesack W (1997) The ammonia monooxygenase structural gene amoA as a functional marker: molecular fine-scale analysis of natural ammonia-oxidizing populations. Appl Environ Microbiol 63:4704–4712

    PubMed Central  CAS  PubMed  Google Scholar 

  45. Leininger S, Urich T, Schloter M, Schwark L, Qi J, Nicol GW, Prosser JI, Schuster SC, Schleper C (2006) Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature 442:806–809

    Article  CAS  PubMed  Google Scholar 

  46. Poly F, Wertz S, Brothier E, Degrange V (2008) First exploration of Nitrobacter diversity in soils by a PCR cloning-sequencing approach targeting functional gene nxrA. FEMS Microbiol Ecol 63:132–140

    Article  CAS  PubMed  Google Scholar 

  47. Wertz S, Poly F, Le Roux X, Degrange V (2008) Development and application of a PCR‐denaturing gradient gel electrophoresis tool to study the diversity of Nitrobacter‐like nxrA sequences in soil. FEMS Microbiol Ecol 63:261–271

    Article  CAS  PubMed  Google Scholar 

  48. Graham DW, Knapp CW, Van Vleck ES, Bloor K, Lane TB, Graham CE (2007) Experimental demonstration of chaotic instability in biological nitrification. ISME J 1:385–393

    Article  CAS  PubMed  Google Scholar 

  49. Erguder TH, Boon N, Wittebolle L, Marzorati M, Verstraete W (2009) Environmental factors shaping the ecological niches of ammonia‐oxidizing archaea. FEMS Microbiol Rev 33:855–869

    Article  CAS  PubMed  Google Scholar 

  50. Zhalnina K, de Quadros PD, Camargo FA, Triplett EW (2012) Drivers of archaeal ammonia-oxidizing communities in soil. Front Microbiol. doi:10.3389/fmicb.2012.00210

    PubMed Central  PubMed  Google Scholar 

  51. Martens-Habbena W, Berube PM, Urakawa H, José R, Stahl DA (2009) Ammonia oxidation kinetics determine niche separation of nitrifying archaea and bacteria. Nature 461:976–979

    Article  CAS  PubMed  Google Scholar 

  52. Taylor AE, Zeglin LH, Wanzek TA, Myrold DD, Bottomley PJ (2012) Dynamics of ammonia-oxidizing archaea and bacteria populations and contributions to soil nitrification potentials. ISME J 6:2024–2032

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  53. Verhamme DT, Prosser JI, Nicol GW (2011) Ammonia concentration determines differential growth of ammonia-oxidising archaea and bacteria in soil microcosms. ISME J 5:1067–1071

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  54. Blackburne R, Vadivelu VM, Yuan Z, Keller J (2007) Kinetic characterisation of an enriched Nitrospira culture with comparison to Nitrobacter. Water Res 41:3033–3042

    Article  CAS  PubMed  Google Scholar 

  55. Schramm A, de Beer D, van den Heuvel JC, Ottengraf S, Amann R (1999) Microscale distribution of populations and activities of Nitrosospira and Nitrospira spp. along a macroscale gradient in a nitrifying bioreactor: quantification by in situ hybridization and the use of microsensors. Appl Environ Microbiol 65:3690–3696

    PubMed Central  CAS  PubMed  Google Scholar 

  56. Wertz S, Leigh AK, Grayston SJ (2012) Effects of long‐term fertilization of forest soils on potential nitrification and on the abundance and community structure of ammonia oxidizers and nitrite oxidizers. FEMS Microbiol Ecol 79:142–154

    Article  CAS  PubMed  Google Scholar 

  57. Nicol GW, Leininger S, Schleper C, Prosser JI (2008) The influence of soil pH on the diversity, abundance and transcriptional activity of ammonia oxidizing archaea and bacteria. Environ Microbiol 10:2966–2978

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank the two anonymous reviewers for their constructive comments that helped to improve the article. We would like to thank the people involved in the initial experimentation from which the soil samples used in the present study were obtained, and in particular Annick Ambroise, Laure Barthes, Juliette Bloor, Sandrine Fontaine and Paul Leadley from the Laboratoire Ecologie, Systématique, Evolution (UMR 8079). Quantitative PCR were performed at the Microbial Ecology Centre (UMR 5557, USC 1364) and DTAMB platform (FR 41, University Lyon 1). This study was funded by AgroParisTech support of the Institute of Ecology and Environmental Sciences - Paris (UMR 7618), and CNRS and INRA supports of UMR 5557 / USC 1364.

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Authors and Affiliations

  1. Institute of Ecology and Environmental Sciences - Paris, UMR 7618 Université Pierre et Marie Curie/CNRS/AgroParisTech, 78850, Thiverval Grignon, France

    Marie Simonin, Naoise Nunan & Audrey Niboyet

  2. Microbial Ecology Center, Université de Lyon/Université Lyon 1/CNRS/INRA, UMR CNRS 5557, USC INRA 1364, 69622, Villeurbanne, France

    Marie Simonin, Xavier Le Roux, Franck Poly & Catherine Lerondelle

  3. Center for Ecosystem Science and Society and Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Bruce A. Hungate

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  1. Marie Simonin
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  3. Franck Poly
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Correspondence to Audrey Niboyet.

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Simonin, M., Le Roux, X., Poly, F. et al. Coupling Between and Among Ammonia Oxidizers and Nitrite Oxidizers in Grassland Mesocosms Submitted to Elevated CO2 and Nitrogen Supply. Microb Ecol 70, 809–818 (2015). https://doi.org/10.1007/s00248-015-0604-9

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